High rates of HCO3– secretion and Cl– absorption against adverse gradients in the marine teleost intestine: the involvement of an electrogenic anion exchanger and H+-pump metabolon?

Grosell, Martin; Mager, Edward M.; Williams, Cameron; Taylor, Janet

doi:10.1242/jeb.027730

Cited by 112 publications

(118 citation statements)

References 93 publications

(137 reference statements)

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“…In essence, freshwater fish must be able to combat water gain and ion loss, while the opposite is true for fish found in saltwater environments. Much is known about the physiological processes involved in ion and water regulation, from branchial, intestinal and renal transport (reviewed by Cerda and Finn, 2010;Grosell et al, 2009;Evans, 2008;Ando et al, 2003;Karnaky, 1998) to hormonal regulation (reviewed by Takei, 2008;Manzon, 2002;McCormick, 2001). There are also many euryhaline species that are able to transition between the two extremes of freshwater and seawater.…”

Section: Introductionmentioning

confidence: 99%

Diet influences salinity preference of an estuarine fish, the killifishFundulus heteroclitus

Bucking

Wood

Grosell

2012

Journal of Experimental Biology

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SUMMARYUnderstanding the interplay among the external environment, physiology and adaptive behaviour is crucial for understanding how animals survive in their natural environments. The external environment can have wide ranging effects on the physiology of animals, while behaviour determines which environments are encountered. Here, we identified changes in the behavioural selection of external salinity in Fundulus heteroclitus, an estuarine teleost, as a consequence of digesting a meal. Fish that consumed high levels of dietary calcium exhibited a higher preferred salinity compared with unfed fish, an effect that was exaggerated by elevated dietary sodium chloride. The mean swimming speed (calculated as a proxy of activity level) was not affected by consuming a diet of any type. Constraining fish to water of 22p.p.t. salinity during the digestion of a meal did not alter the amount of calcium that was absorbed across the intestine. However, when denied the capacity to increase their surrounding salinity, the compromised ability to excrete calcium to the water resulted in significantly elevated plasma calcium levels, a potentially hazardous physiological consequence. This study is the first to show that fish behaviourally exploit their surroundings to enhance their ionoregulation during digestion, and to pinpoint the novel role of dietary calcium and sodium in shaping this behaviour. We conclude that in order to resolve physiological disturbances in ion balance created by digestion, fish actively sense and select the environment they inhabit. Ultimately, this may result in transient diet-dependent alteration of the ecological niches occupied by fishes, with broad implications for both physiology and ecology.

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Section: Introductionmentioning

confidence: 99%

Diet influences salinity preference of an estuarine fish, the killifishFundulus heteroclitus

Bucking

Wood

Grosell

2012

Journal of Experimental Biology

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“…moll -1 DIDS, inhibition of HCO 3 -excretion was also not observed in O. mykiss (Wilson et al, 1996). It has been noted that the preparation of DIDS is key to its efficacy (Grosell et al, 2009b), and such precautions were taken in the present study. We thus conclude that the HCO 3 -excretion mechanism is relatively DIDS insensitive in loach and similar to that seen in trout and flounder (Grosell et al, 1999;Grosell et al, 2009a).…”

Section: Gut Membrane Fluiditymentioning

confidence: 99%

“…The NHE isoform 1 (NHE1) is expressed at the basolateral membrane, whereas NHE2 is apical and NHE3 is recycled between intracellular vesicles and the plasma membrane (Zachos et al, 2005). Gut lumen surface alkalinization in the loach is probably accomplished through HCO 3 -excretion in exchange for Cl -as has been reported in marine fishes (Grosell et al, 2009b). Although intestinal base excretion has been reported in freshwater trout (Genz et al, 2011), the mechanism of luminal alkalinizaton has only been well characterized in marine fishes, which imbibe water for osmoregulation (Grosell, 2006).…”

Section: Introductionmentioning

confidence: 95%

“…Although intestinal base excretion has been reported in freshwater trout (Genz et al, 2011), the mechanism of luminal alkalinizaton has only been well characterized in marine fishes, which imbibe water for osmoregulation (Grosell, 2006). The intestinal anion exchanger responsible for alkalinization in marine teleosts has been determined to be Slc26a6 (Kurita et al, 2008;Grosell et al, 2009b) although in freshwater trout gut expression is generally absent (Genz et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Mechanisms of transepithelial ammonia excretion and luminal alkalinization in the gut of an intestinal air-breathing fish, Misgurnus anguilliacaudatus

Wilson

Moreira‐Silva

Delgado

et al. 2012

Journal of Experimental Biology

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-1). Carbonic anhydrase does not appear to be associated with gut alkalinization under these conditions as ethoxzolamide was without effect on J base . Membrane fluidity of the posterior intestine was low, suggesting low permeability, which was also reflected in a lower mucosal-serosal J amm in the presence of an imposed gradient, in contrast to that in the anterior intestine. To conclude, although the posterior intestine is highly modified for gas exchange, it is the anterior intestine that is the likely site of ammonia excretion and alkalinization leading to ammonia volatilization in the gut. Supplementary material available online at

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“…Unlike freshwater fishes, however, seawater fishes experience passive water efflux. To balance water loss, seawater fishes absorb water and ions through the intestine by drinking large amounts of seawater (17). Surplus ions are excreted mainly through the gills (13,22), although divalent ions (Mg 2ϩ and SO 4 2Ϫ ) are excreted through isotonic urine (4,30).…”

mentioning

confidence: 99%

Differential expression of Na⁺-Cl⁻cotransporter and Na⁺-K⁺-Cl⁻cotransporter 2 in the distal nephrons of euryhaline and seawater pufferfishes

Kato

Muro

Kimura

et al. 2011

American Journal of Physiology-Regulatory, Integrative and Comp

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in the distal nephrons of euryhaline and seawater pufferfishes. Am J Physiol Regul Integr Comp Physiol 300: R284 -R297, 2011. First published November 17, 2010 doi:10.1152/ajpregu.00725.2009.-The process of NaCl reabsorption in the distal nephron allows freshwater fishes to excrete hypotonic urine and seawater fishes to excrete urine containing high concentrations of divalent ions; the relevant transporters, however, have not yet been identified. In the mammalian distal nephron, NaCl absorption is mediated by Na ϩ -K ϩ -Cl Ϫ cotransporter 2 (NKCC2, Slc12a1) in the thick ascending limb, Na ϩ -Cl Ϫ cotransporter (NCC, Slc12a3) in the distal convoluted tubule, and epithelial sodium channel (ENaC) in the collecting duct. In this study, we compared the expression profiles of these proteins in the kidneys of euryhaline and seawater pufferfishes. Mining the fugu genome identified one NKCC2 gene and one NCC gene, but no ENaC gene. RT-PCR and in situ hybridization analyses demonstrated that NKCC2 was highly expressed in the distal tubules and NCC was highly expressed in the collecting ducts of euryhaline pufferfish (mefugu, Takifugu obscurus). On the other hand, the kidney of seawater pufferfish (torafugu, Takifugu rubripes), which lacked distal tubules, expressed very low levels of NCC, and, in the collecting ducts, high levels of NKCC2. Acclimation of mefugu to seawater resulted in a 2.7ϫ decrease in NCC expression, whereas NKCC2 expression was not markedly affected. Additionally, internalization of NCC from the apical surface of the collecting ducts was observed. These results suggest that NaCl reabsorption in the distal nephron of the fish kidney is mediated by NCC and NKCC2 in freshwater and by NKCC2 in seawater. distal tubule; collecting duct; NKCC2; NCC; fish kidney; dilute urine FRESHWATER FISHES LIVE IN hypo-osmotic environments, resulting in significant influx of water into the body, mainly across the gills. To maintain body fluid homeostasis, freshwater fishes import ions from surrounding water through the gills (13,22) or from the diet, and excrete excess water in hypotonic urine (ϳ10 mM Na ϩ and Cl Ϫ ) through the kidneys (30). To increase urine volume (i.e., water excretion), freshwater fishes secrete NaCl in the proximal tubule and draw interstitial water into the tubular lumen (9); this proximally introduced NaCl should be reabsorbed in the distal nephron. Reabsorption of Na ϩ and Cl Ϫ ions from urine under water-impermeable conditions is, therefore, essential for net water excretion and the survival of fishes in freshwater. Na ϩ and Cl Ϫ reabsorption is also important for seawater fishes. Unlike freshwater fishes, however, seawater fishes experience passive water efflux. To balance water loss, seawater fishes absorb water and ions through the intestine by drinking large amounts of seawater (17). Surplus ions are excreted mainly through the gills (13, 22), although divalent ions (Mg 2ϩ and SO 4 2Ϫ ) are excreted through isotonic urine (4, 30). To produce urine with high concentrations of Mg 2ϩ (ϳ140 mM) ...

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High rates of HCO3– secretion and Cl– absorption against adverse gradients in the marine teleost intestine: the involvement of an electrogenic anion exchanger and H+-pump metabolon?

Abstract: SummaryAnion exchange contributes significantly to intestinal Cl -absorption in marine teleost fish and is thus vital for successful osmoregulation. This anion exchange process leads to high luminal HCO 3 -concentrations (up to ~100 mmol l

Cited by 112 publications

References 93 publications

Diet influences salinity preference of an estuarine fish, the killifishFundulus heteroclitus

Diet influences salinity preference of an estuarine fish, the killifishFundulus heteroclitus

Mechanisms of transepithelial ammonia excretion and luminal alkalinization in the gut of an intestinal air-breathing fish, Misgurnus anguilliacaudatus

Differential expression of Na⁺-Cl⁻cotransporter and Na⁺-K⁺-Cl⁻cotransporter 2 in the distal nephrons of euryhaline and seawater pufferfishes

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High rates of HCO3– secretion and Cl– absorption against adverse gradients in the marine teleost intestine: the involvement of an electrogenic anion exchanger and H+-pump metabolon?

Abstract: SummaryAnion exchange contributes significantly to intestinal Cl -absorption in marine teleost fish and is thus vital for successful osmoregulation. This anion exchange process leads to high luminal HCO 3 -concentrations (up to ~100 mmol l

Cited by 112 publications

References 93 publications

Diet influences salinity preference of an estuarine fish, the killifishFundulus heteroclitus

Diet influences salinity preference of an estuarine fish, the killifishFundulus heteroclitus

Mechanisms of transepithelial ammonia excretion and luminal alkalinization in the gut of an intestinal air-breathing fish, Misgurnus anguilliacaudatus

Differential expression of Na+-Cl−cotransporter and Na+-K+-Cl−cotransporter 2 in the distal nephrons of euryhaline and seawater pufferfishes

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Differential expression of Na⁺-Cl⁻cotransporter and Na⁺-K⁺-Cl⁻cotransporter 2 in the distal nephrons of euryhaline and seawater pufferfishes